Complexities of nitrogen isotope biogeochemistry in plant-soil systems: Implications for the study of ancient agricultural and animal management practices

Frontiers in Plant Science

Volumn 5, Issue JUN, 2014, Pages

  Szpak, Paul ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Agriculture; Animal management; Archaeology; Nitrogen; Stable isotopes

Indexed keywords

EID: 84979517980     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2014.00288     Document Type: Review

References (195)

1. 4 from dairy cows housed in a farmyard manure tying stall (housing, manure storage, manure spreading). Nutr. Cycl. Agroecosys. 60, 103-113. doi: 10.1023/A:1012649028772
2. Amundson, R., Austin, A. T., Schuur, E. A. G., Yoo, K., Matzek, V., Kendall, C., et al. (2003). Global patterns of the isotopic composition of soil and plant nitrogen. Global Biogeochem. Cycl. 17, 1031. doi: 10.1029/2002gb001903
3. 4 plants along land use gradients in southern Africa. J. AridEnviron. 72, 326-337. doi: 10.1016/j.jaridenv.2007.06.007
4. 15 is negativelycorrelated with rainfall along the IGBP transect in Australia. Aust. J. Plant Physiol. 26, 293-298. doi: 10.1071/PP98144
5. Austin, A. T., and Vitousek, P. M. (1998). Nutrient dynamics on a precipitation gradient in Hawai'i. Oecologia 113, 519-529. doi: 10.1007/s004420050405
6. Bardgett, R. D., and Wardle, D. A. (2003). Herbivore-mediated linkages between aboveground and belowground communities. Ecology 84, 2258-2268. doi: 10.1890/02-0274
7. Bateman, A. S., and Kelly, S. D. (2007). Fertilizer nitrogen isotope signatures. Isot. Environ. andHealthStud. 43,237-247. doi: 10.1080/10256010701550732
8. Bateman, A. S., Kelly, S. D., and Jickells, T. D. (2005). Nitrogen isotope relationships between crops and fertilizer: implications for using nitrogen isotope analysis as an indicator of agricultural regime. J. Agric. Food Chem. 53, 5760-5765. doi: 10.1021/jf050374h
9. 15N) detect effects of wildfires on tree physiological processes in Pinus sylvestris L. Trees 25, 627-636. doi: 10.1007/s00468-011-0539-9
10. Bocherens, H., Polet, C., and Toussaint, M. (2007). Palaeodiet of Mesolithic and Neolithic populations of Meuse Basin (Belgium): evidence from stable isotopes. J. Archaeol. Sci. 34, 10-27. doi: 10.1016/j.jas.2006.03.009
11. Bogaard, A. (2002). Questioning the relevance of shifting cultivation to Neolithic farming in the loess belt of Europe: evidence from the Hambach Forest experiment. Veg. Hist. Archaeobot. 11, 155-168. doi: 10.1007/s003340200017
12. Bogaard, A., Fraser, R., Heaton, T. H. E., Wallace, M., Vaiglova, P., Charles, M., et al. (2013). Crop manuring and intensive land management by Europe's first farmers. Proc. Natl. Acad. Sci. U.S.A. 110, 12589-12594. doi: 10.1073/pnas.1305918110
13. Bogaard, A., Heaton, T. H. E., Poulton, P., and Merbach, I. (2007). The impact of manuring on nitrogen isotope ratios in cereals: archaeological implications for reconstruction of diet and crop management practices. J. Archaeol. Sci. 34, 335-343. doi: 10.1016/j.jas.2006.04.009
14. Borić, D., and Price, T. D. (2013). Strontium isotopes document greater human mobility at the start of the Balkan Neolithic. Proc. Natl. Acad. Sci. U.S.A. 110, 3298-3303. doi: 10.1073/pnas.1211474110
15. Britton, K., Müldner, G., and Bell, M. (2008). Stable isotope evidence for salt-marsh grazing in the Bronze Age Severn Estuary, UK: implications for palaeodietary analysis at coastal sites. J. Archaeol. Sci. 35, 2111-2118. doi: 10.1016/j.jas.2008.01.012
16. Broadbent, F. E., Rauschkolb, R. S., Lewis, K. A., and Chang, G. Y. (1980). Spatial variability of nitrogen-15 and total nitrogen in some virgin and cultivated soils. Soil Sci. Soc. Am. J. 44, 524-527. doi: 10.2136/sssaj1980.03615995004400030017x
17. Brundrett, M. (2009). Mycorrhizal associations and other means of nutrition of vascular plants: understanding the global diversity of host plants by resolving conflicting information and developing reliable means of diagnosis. Plant Soil 320, 37-77. doi: 10.1007/s11104-008-9877-9
18. 13C): the effect of diet isotopic values and applications for diet reconstruction. J. Appl. Ecol. 46, 443-453. doi: 10.1111/j.1365-2664.2009.01620.x
19. Charles, M., Halstead, P., and Jones, G. (1996). The archaeology of fodder: introduction. Environ. Archaeol. 1, i-ii. doi: 10.1179/env.1996.1.1.i
20. 15N of crops applied with organic and chemical fertilizers in a four-year rotation. Plant Soil 284, 165-174. doi: 10.1007/s11104-006-0038-8
21. 15N abundances of maize and soil amended with urea and composted pig manure. PlantSoil245, 223-232. doi: 10.1023/A:1020475017254
22. 15N in soils and plants from chemically and organically fertilized uplands. Soil Biol. Biochem. 35, 1493-1500. doi: 10.1016/S0038-0717(03)00246-3
23. 15N-urea as affected bythe co-application of composted pig manure. Can. J. Soil Sci. 87, 485-493. doi: 10.4141/CJSS07002
24. Clementz, M. T. (2012). New insight from old bones: stable isotope analysis of fossil mammals. J. Mammal. 93, 368-380. doi: 10.1644/11-MAMM-S-179.1
25. 15N compositions along the ruminant gastrointestinal tract: does digestion influence the relationship between diet and faeces? Eur. J. Wildlife Res. 58, 303-313. doi: 10.1007/s10344-011-0581-3
26. Coetsee, C., Stock, W. D., and Craine, J. M. (2011). Do grazers alter nitrogen dynamics on grazing lawns in a South African savannah? Afr. J. Ecol. 49, 62-69. doi: 10.1111/j.1365-2028.2010.01236.x
27. 15N values reflect ancient human activity. J. Archaeol. Sci. 33, 1167-1176. doi: 10.1016/j.jas.2005.12.005
28. Cook, G. D. (2001). Effects of frequent fires and grazing on stable nitrogen isotope ratios of vegetation in northern Australia. Austral Ecol. 26, 630-636. doi: 10.1046/j.1442-9993.2001.01150.x
29. Craine, J. M., Ballantyne, F., Peel, M., Zambatis, N., Morrow, C., and Stock, W. D. (2009a). Grazing and landscape controls on nitrogen availability across 330 South African savanna sites. Austral Ecol. 34, 731-740. doi: 10.1111/j.1442-9993.2009.01978.x
30. Craine, J. M., Elmore, A. J., Aidar, M. P. M., Bustamante, M., Dawson, T. E., Hobbie, E. A., et al. (2009b). Global patterns of foliar nitrogen isotopes and their relationships with climate, mycorrhizal fungi, foliar nutrient concentrations, and nitrogen availability. New Phytol. 183, 980-992. doi: 10.1111/j.1469-8137.2009.02917.x
31. Del Amor, F. M., Navarro, J., and Aparicio, P. M. (2008). Isotopic discrimination as a tool for organic farming certification in sweet pepper. J. Environ. Qual. 37, 182-185. doi: 10.2134/jeq2007.0329
32. DeNiro, M. J., andEpstein, S. (1978). Influence of diet on the distribution ofcarbon isotopes in animals. Geochim. Cosmochim. Acta 42, 495-506. doi: 10.1016/0016-7037(78)90199-0
33. DeNiro, M. J., and Epstein, S. (1981). Influence of diet on the distribution of nitrogen isotopes in animals. Geochim. Cosmochim. Acta 45, 341-351. doi: 10.1016/0016-7037(81)90244-1
34. 12C ratios of plant matter during the initial stages of diagenesis: studies utilizing archaeological specimens from Peru. Geochim. Cosmochim. Acta 49, 97-115. doi: 10.1016/0016-7037(85)90194-2
35. Eghball, B., Wienhold, B. J., Gilley, J. E., and Eigenberg, R. A. (2002). Mineralization of manure nutrients. J. Soil Water Conserv. 57, 470-473.
36. 15N in forests across a nitrogen deposition gradient. Forest Ecol. Manag. 101, 9-18. doi: 10.1016/s0378-1127(97) 00121-7
37. Erickson, A. E. (1982). “Tillage effects on soil aeration," in Predicting Tillage Effects on Soil Physical Properties and Processes. ASA Special Publication 44, eds P. W. Unger and D. M. Van Doren Jr. (Madison, WI: American Society of Agronomy and Soil Science Society ofAmerica), 91-104.
38. 15N natural abundance. Oecologia 117, 187-193. doi: 10.1007/s004420050647
39. Evans, R. D. (2001). Physiological mechanisms influencing plant nitrogen isotope composition. Trends Plant Sci. 6,121-126. doi: 10.1016/S1360-1385(01)01889-1
40. Evans, R. D., Bloom, A. J., Sukrapanna, S. S., and Ehleringer, J. R. (1996). Nitrogen isotope composition of tomato (Lycopersicon esculentum Mill. cv. T-5) grown under ammonium or nitrate nutrition. Plant Cell Environ. 19, 1317-1323. doi: 10.1111/j.1365-3040.1996.tb00010.x
41. Finlay, R. D. (2008). Ecological aspects of mycorrhizal symbiosis: with special emphasis on the functional diversity of interactions involving the extraradical mycelium. J. Exp. Bot. 59, 1115-1126. doi: 10.1093/jxb/ern059
42. Finucane, B., Agurto, P. M., and Isbell, W. H. (2006). Human and animal diet at Conchopata, Peru: stable isotope evidence for maize agriculture and animal management practices during the Middle Horizon. J. Archaeol. Sci. 33, 1766-1776. doi: 10.1016/j.jas.2006.03.012
43. 15N) of mangroves and lichens in an oligotrophic, microbially-influenced ecosystem. Biogeosciences 5, 1693-1704. doi: 10.5194/bg-5-1693-2008
44. 15N abundance of a grazed grassland. Biogeochemistry 68, 169-178. doi: 10.1023/b:biog.0000025736.19381.91
45. Frank, D., and Zhang, Y. (1997). Ammonia volatilization from a seasonally and spatially variable grazed grassland: Yellowstone National Park. Biogeochemistry 36, 189-203. doi: 10.1023/A:1005705121160
46. Frank, D. A., and Evans, R. D. (1997). Effects of native grazers on grassland in cycling in Yellowstone National Park. Ecology 78, 2238-2248. doi: 10.1890/0012-9658(1997)078[2238:eongog]2.0.co;2
47. Fraser, R. A., Bogaard, A., Charles, M., Styring, A. K., Wallace, M., Jones, G., et al. (2013). Assessing natural variation and the effects of charring, burial and pretreatment on the stable carbon and nitrogen isotope values of archaeobotanical cereals and pulses. J. Archaeol. Sci. 40, 4754-4766. doi: 10.1016/j.jas.2013. 01.032
48. Fraser, R. A., Bogaard, A., Heaton, T., Charles, M., Jones, G., Christensen, B. T., et al. (2011). Manuring and stable nitrogen isotope ratios in cereals and pulses: towards a new archaeobotanical approach to the inference of land use and dietary practices. J. Archaeol. Sci. 38, 2790-2804. doi: 10.1016/j.jas.2011.06.024
49. 15N values in nitrogenous compounds from Brassica napus L. leaves. Plant Cell Environ. 36, 128-137. doi: 10.1111/j.1365-3040.2012.02561.x
50. Gebauer, G., Giesemann, A., Schulze, E., and Jäger, H. (1994). Isotope ratios and concentrations of sulfur and nitrogen in needles and soils of Picea abies stands as influenced by atmospheric deposition of sulfur and nitrogen compounds. PlantSoil 164, 267-281. doi: 10.1007/bf00010079
51. Gonzalvez, A., Armenta, S., and De La Guardia, M. (2009). Trace-element composition and stable-isotope ratio for discrimination of foods with protected designation of origin. Trends Anal. Chem. 28, 1295-1311. doi: 10.1016/j.trac.2009.08.001
52. Gosling, P., Hodge, A., Goodlass, G., and Bending, G. D. (2006). Arbuscular mycorrhizal fungi and organic farming. Agric. Ecosyst. Environ. 113, 17-35. doi: 10.1016/j.agee.2005.09.009
53. Grogan, P., Burns, T. D., and Chapin, F. S. 3rd. (2000). Fire effects on ecosystem nitrogen cycling in a Californian bishop pine forest. Oecologia 122, 537-544. doi: 10.1007/s004420050977
54. Gustine, D. D., Barboza, P. S., Adams, L. G., Farnell, R. G., and Parker, K. L. (2011). An isotopic approach to measuring nitrogen balance in caribou. J. Wildlife Manag. 75, 178-188. doi: 10.1002/jwmg.11
55. Gustine, D. D., Barboza, P. S., and Lawler, J. P. (2010). Dynamics of body protein and the implications for reproduction in captive muskoxen (Ovibos moschatus) during winter. Physiol. Biochem. Zool. 83, 687-697. doi: 10.1086/652729
56. Han, G., Hao, X., Zhao, M., Wang, M., Ellert, B. H., Willms, W., et al. (2008). Effect of grazing intensity on carbon and nitrogen in soil and vegetation in a meadow steppe in Inner Mongolia. Agric. Ecosyst. Environ. 125, 21-32. doi: 10.1016/j.agee.2007.11.009
57. 15N) of ecosystem samples reflects measures of water availability. Aust. J. Plant Physiol. 26, 185-199. doi: 10.1071/PP98146
58. 15N natural abundance: the present limits to interpretation for uncultivated systems with original data from a Scottish old field. Adv. Ecol. Res. 27, 133-212.
59. 15N in soil and plants at a New Zealand hill country site: correlations with soil chemistry and nutrient inputs. Aust. J. Soil Res. 39, 373-383. doi: 10.1071/SR99094
60. Herman, D. J., and Rundel, P. W. (1989). Nitrogen isotope fractionation in burned and unburned chaparral soils. Soil Sci. Soc. Am. J. 53, 1229-1236. doi: 10.2136/sssaj1989.03615995005300040040x
61. Hobbie, E., and Ouimette, A. (2009). Controls of nitrogen isotope patterns in soil profiles. Biogeochemistry 95, 355-371. doi: 10.1007/s10533-009-9328-6
62. Hobbie, E. A., and Agerer, R. (2010). Nitrogen isotopes in ectomycorrhizal sporo-carps correspond to belowground exploration types. Plant Soil 327, 71-83. doi: 10.1007/s11104-009-0032-z
63. Hobbie, E. A., and Högberg, P. (2012). Nitrogen isotopes link mycorrhizal fungi and plants to nitrogen dynamics. NewPhytol. 196, 367-382. doi: 10.1111/j.1469-8137.2012.04300.x
64. Hobbie, E. A., Macko, S. A., and Shugart, H. H. (1999). Insights into nitrogen and carbon dynamics of ectomycorrhizal and saprotrophic fungi from isotopic evidence. Oecologia 118, 353-360. doi: 10.1007/s004420050736
65. Hobbs, N. T. (1996). Modification of ecosystems by Ungulates. J. Wildlife Manag. 60, 695-713. doi: 10.2307/3802368
66. 15N natural abundance in soil-plant systems.NewPhytol. 137, 179-203. doi: 10.1046/j.1469-8137.1997.00808.x
67. 15N abundance of surface soils, roots and mycor-rhizas in profiles of European forest soils. Oecologia 108, 207-214. doi: 10.1007/bf00334643
68. 15N Abundance of forests is correlated with losses of nitrogen. PlantSoil 157, 147-150. doi: 10.1007/BF02390237
69. 15N natural abundance of trees in N-loaded forests caused by an internal ecosystem N isotope redistribution or a change in the ecosystem N isotope mass balance? Biogeochemistry 117, 351-358. doi: 10.1007/s10533-013-9873-x
70. Högberg, P., Johannisson, C., Yarwood, S., Callesen, I., Näsholm, T., Myrold, D. D., et al. (2011). Recovery of ectomycorrhiza after ‘nitrogen saturation' of a conifer forest. NewPhytol. 189, 515-525. doi: 10.1111/j.1469-8137.2010.03485.x
71. Huber, E., Bell, T., and Adams, M. (2013). Combustion influences on natural abundance nitrogen isotope ratio in soil and plants following awildfire in asub-alpine ecosystem. Oecologia 173, 1063-1074. doi: 10.1007/s00442-013-2665-0
72. 13C values of feces reflect the isotopic composition of diets in small mammals? Can. J. Zool. 85, 388-396. doi: 10.1139/z07-019
73. Jensen, A., and Jakobsen, I. (1980). The occrrence of vesicular-arbuscular mycor-rhiza in barley and wheat grown in some Danish soils with different fertilizer treatments. Plant Soil 55, 403-414. doi: 10.1007/BF02182701
74. Johnson, B. G., Johnson, D. W., Chambers, J. C., and Blank, R. R. (2011). Fire effects on the mobilization and uptake of nitrogen by cheatgrass (Bromus tectorum L.). PlantSoil 341, 437-445. doi: 10.1007/s11104-010-0656-z
75. Jones, G. (1996). Distinguishing food from fodder in the archaeobotanical record. Environ. Archaeol. 1,95-98.
76. Jones, R., (ed.). (2012). Manure Matters: Historical, Archaeological and Ethnographic Perspectives. Surrey: Ashgate.
77. Juo, A. S. R., and Manu, A. (1996). Chemical dynamics in slash-and-burn agriculture. Agric. Ecosyst. Environ. 58, 49-60. doi: 10.1016/0167-8809(95)00656-7
78. Kabir, Z., O'Halloran, I. P., Fyles, J. W., and Hamel, C. (1997). Seasonal changes of arbuscular mycorrhizal fungi as affected by tillage practices and fertilization: hyphal density and mycorrhizal root colonization. Plant Soil 192, 285-293. doi: 10.1023/A:1004205828485
79. Kahiluoto, H., Ketoja, E., Vestberg, M., and Saarela, I. (2001). Promotion of AM utilization through reduced P fertilization 2. Field studies. PlantSoil 231, 65-79. doi: 10.1023/A:1010366400009
80. 15N at natural abundance. Plant Methods 9, 27. doi: 10.1186/1746-4811-9-27
81. 15N analyses of charred cereal grains from the 4th to the 1st millennium BC. J. Archaeol. Sci. doi: 10.1016/j.jas.2013.04.018
82. 15N signatures in archaeobotanical material. J. Archaeol. Sci. 39, 2533-2540. doi: 10.1016/j.jas.2012.03.007
83. Karamanos, R. E., Voroney, R. P., and Rennie, D. A. (1981). Variation in natural N-15 abundance of central Saskatchewan soils. Soil Sci. Soc. Am. J. 45, 826-828. doi: 10.2136/sssaj1981.03615995004500040031x
84. Keegan, W. F., and DeNiro, M. J. (1988). Stable carbon-and nitrogen-isotope ratios of bone collagen used to study coral-reef and terrestrial components of prehistoric Bahamian diet. Am. Antiq. 53,320-336. doi: 10.2307/281022
85. Kellner, C. M., and Schoeninger, M. J. (2007). A simple carbon isotope model for reconstructing prehistoric human diet. Am. J. Phys. Anthropol. 133, 1112-1127. doi: 10.1002/ajpa.20618
86. Kim, Y.-J., Choi, W.-J., Lim, S.-S., Kwak, J.-H., Chang, S. X., Kim, H.-Y., et al. (2008). Changes in nitrogen isotopic compositions during composting of cattle feedlot manure: effects of bedding material type. Bioresour. Technol. 99, 5452-5458. doi: 10.1016/j.biortech.2007.11.012
87. Kirchmann, H. (1985). Losses, plant uptake and utilisation of manure nitrogen during a production cycle. Acta Agric. Scand. Suppl. 24, 5-77.
88. Klopatek, J. M., Klopatek, C. C., and DeBano, L. F. (1990). Potential variation of nitrogen transformations in pinyon-juniper ecosystems resulting from burning. Biol. Fertil. Soils 10, 35-44. doi: 10.1007/BF00336122
89. Knobbe, N., Vogl, J., Pritzkow, W., Panne, U., Fry, H., Lochotzke, H., et al. (2005). C and N stable isotope variation in urine and milk of cattle depending on the diet. Anal. Bioanal. Chem. 386, 104-108. doi: 10.1007/s00216-006-0644-6
90. Kolb, K. J., and Evans, R. D. (2002). Implications of leaf nitrogen recycling on the nitrogen isotope composition of deciduous plant tissues. New Phytol. 156, 57-64. doi: 10.1046/j.1469-8137.2002.00490.x
91. 15N abundance in two nitrogen saturated forest ecosystems. Oecologia 111, 470-480. doi: 10.1007/s004420050260
92. Kreitler, C. W., and Jones, D. C. (1975). Natural soil nitrate: the cause of the nitrate contamination of ground water in Runnels County, Texasa. Ground Water 13, 53-62. doi: 10.1111/j.1745-6584.1975.tb03065.x
93. 15N abundance. Agric. Ecosyst. Environ. 184, 158-167. doi: 10.1016/j.agee.2013.11.028
94. Laird, D., Fleming, P., Wang, B., Horton, R., and Karlen, D. (2010). Biochar impact on nutrient leaching from a Midwestern agricultural soil. Geoderma 158, 436-442. doi: 10.1016/j.geoderma.2010.05.012
95. 15N in the profiles of some Australian pasture soils. Aust. J. Soil Res. 22, 155-164. doi: 10.1071/sr9840155
96. 15N indicates shifts in plant nitrogen acquisition after severe wildfire and through forest stand development. Plant Soil 373, 955-965. doi: 10.1007/s11104-013-1856-0
97. Lehmann, J., Pereira Da Silva, J. Jr., Steiner, C., Nehls, T., Zech, W., and Glaser, B. (2003). Nutrient availability and leaching in an archaeological Anthrosol and a Ferralsol of the Central Amazon basin: fertilizer, manure and charcoal amendments. Plant Soil 249, 343-357. doi: 10.1023/A:1022833116184
98. 15N value to long-term stocking rates on a rough fescue grassland. Soil Sci. Plant Nutr. 58, 326-333. doi: 10.1080/00380768.2012.682283
99. Li, C., Hao, X., Willms, W. D., Zhao, M., and Han, G. (2009). Seasonal response of herbage production and its nutrient and mineral contents to long-term cattle grazing on a Rough Fescue grassland. Agric. Ecosyst. Environ. 132, 32-38. doi: 10.1016/j.agee.2009.02.010
100. Li, C., Hao, X., Zhao, M., Han, G., and Willms, W. D. (2008). Influence of historic sheep grazing on vegetation and soil properties of a Desert Steppe in Inner Mongolia. Agric. Ecosyst. Environ. 128, 109-116. doi: 10.1016/j.agee.2008.05.008
101. Lightfoot, E., and Stevens, R. E. (2012). Stable isotope investigations of charred barley (Hordeum vulgare) and wheat (Triticum spelta) grains from Danebury Hillfort: implications for palaeodietary reconstructions. J. Archaeol. Sci. 39, 656-662. doi: 10.1016/j.jas.2011.10.026
102. Lim, S.-S., Choi, W.-J., Kwak, J.-H., Jung, J.-W., Chang, S., Kim, H.-Y., et al. (2006). Nitrogen and carbon isotope responses of Chinese cabbage and chrysanthemum to the application of liquid pig manure. Plant Soil 295, 67-77. doi: 10.1007/s11104-007-9262-0
103. Lindwall, F., Vowles, T., Ekblad, A., and Björk, R. G. (2013). Reindeer grazing has contrasting effect on species traits in Vaccinium vitis-idaea L. and Bistorta vivipara (L.) Gray. Acta Oecologica 53, 33-37. doi: 10.1016/j.actao.2013.08.006
104. Macko, S. A., Engel, M. H., and Qian, Y. (1994). Early diagenesis and organic matter preservation-a molecular stable carbon isotope perspective. Chem. Geol. 114, 365-379. doi: 10.1016/0009-2541(94)90064-7
105. Macko, S. A., Estep, M. L. F., Engel, M. H., and Hare, P. E. (1986). Kinetic fractionation of stable nitrogen isotopes during amino acid transamination. Geochim. Cosmochim. Acta 50, 2143-2146. doi: 10.1016/0016-7037(86)90068-2
106. Madgwick, R., Mulville, J., and Stevens, R. E. (2012). Diversity in foddering strategy and herd management in late Bronze Age Britain: an isotopic investigation of pigs and other fauna from two midden sites. Environm. Archaeol. 17, 126-140. doi: 10.1179/1461410312Z.00000000011
107. Mae, T., and Ohira, K. (1981). The remobilization of nitrogen related to leaf growth and senescence in rice plants (Oryzasativa L.). Plant Cell Physiol. 22, 1067-1074.
108. 13C) isotopes in sheep dentinal collagen. J. Archaeol. Sci. 41, 502-510. doi: 10.1016/j.jas.2013. 09.016
109. Martinelli, L. A., Piccolo, M. C., Townsend, A. R., Vitousek, P. M., Cuevas, E., McDowell, W., et al. (1999). Nitrogen stable isotopic composition of leaves and soil: tropical versus temperate forests. Biogeochemistry 46, 45-65. doi: 10.1023/a:1006100128782
110. Martre, P., Porter, J. R., Jamieson, P. D., and Triboï, E. (2003). Modeling grain nitrogen accumulation and protein composition to understand the sink/source regulations of nitrogen remobilization for wheat. Plant Physiol. 133, 1959-1967. doi: 10.1104/pp.103.030585
111. Matson, P. A., Parton, W. J., Power, A. G., and Swift, M. J. (1997). Agricultural intensification and ecosystem properties. Science 277, 504-509. doi: 10.1126/sci-ence.277.5325.504
112. McLauchlan, K. K., Craine, J. M., Oswald, W. W., Leavitt, P. R., and Likens, G. E. (2007). Changes in nitrogen cycling during the past century in a northern hardwood forest. Proc. Natl. Acad. Sci. U.S.A. 104, 7466-7470. doi: 10.1073/pnas.0701779104
113. McNaughton, S. J., Ruess, R. W., and Seagle, S. W. (1988). Large mammals and process dynamics in African ecosystems. Bioscience 38, 794-800. doi: 10.2307/1310789
114. Moore, J. W., and Semmens, B. X. (2008). Incorporating uncertainty and prior information into stable isotope mixing models. Ecol. Lett. 11, 470-480. doi: 10.1111/j.1461-0248.2008.01163.x
115. 15N abundance of vegetation and soil in the Kapalga savanna, Australia. Aust. J. Ecol. 21, 336-340. doi: 10.1111/j.1442-9993.1996.tb00617.x
116. Mozafar, A., Anken, T., Ruh, R., and Frossard, E. (2000). Tillage intensity, mycorrhizal and nonmycorrhizal fungi, and nutrient concentrations in maize, wheat, and canola. Agron. J. 92, 1117-1124. doi: 10.2134/agronj2000. 9261117x
117. 15N abundance in pastoral soils receiving differing amounts of superphosphate fertilizer and irrigation for 50 years. Soil Sci. Soc. Am. J. 77, 830-841. doi: 10.2136/sssaj2012.0333
118. Müldner, G., Britton, K., and Ervynck, A. (2014). Inferring animal husbandry strategies in coastal zones through stable isotope analysis: new evidence from the Flemish coastal plain (Belgium, 1st-15th century AD). J. Archaeol. Sci. 41, 322-332. doi: 10.1016/j.jas.2013.08.010
119. Müldner, G., and Richards, M. P. (2005). Fast or feast: reconstructing diet in later Medieval England by stable isotope analysis. J. Archaeol. Sci. 32, 39-48. doi: 10.1016/j.jas.2004.05.007
120. 15N and water availability. Funct. Ecol. 20, 1062-1069. doi: 10.1111/j.1365-2435.2006.01186.x
121. 15N natural abundances and N use by tundra plants. Oecologia 107, 386-394. doi: 10.1007/bf00328456
122. Nadelhoffer, K. J., and Fry, B. (1994). “Nitrogen isotope studies in forest ecosystems," in Stable Isotopes in Ecology and Environmental Science, eds K. Lathja and R. H. Michener (Oxford: Blackwell Scientific), 22-44.
123. Naito, Y. I., Honch, N. V., Chikaraishi, Y., Ohkouchi, N., and Yoneda, M. (2010). Quantitative evaluation of marine protein contribution in ancient diets based on nitrogen isotope ratios of individual amino acids in bone collagen: an investigation at the Kitakogane Jomon site. Am. J. Phys. Anthropol. 143, 31-40. doi: 10.1002/ajpa.21287
124. Nájera-Hillman, E., and Mandujano, S. (2013). Faecal stable isotope analysis in white-tailed deer (Odocoileusvirginianus), an alternative method for alimentary ecology studies. Wildlife Biol. Pract. 9, 63-75. doi: 10.2461/wbp.2013.9.8
125. 15N values of tomato. Jpn. Agric. Res. Q. 41, 219-226. doi: 10.6090/jarq.41.219
126. Näsholm, T. (1994). Removal of nitrogen during needle senescence in Scots pine (Pinus sylvestris L.). Oecologia 99, 290-296. doi: 10.1007/bf00627741
127. Neilson, R., Hamilton, D., Wishart, J., Marriott, C. A., Boag, B., Handley, L. L., et al. (1998). Stable isotope natural abundances of soil, plants and soil invertebrates in an upland pasture. Soil Biol. Biochem. 30, 1773-1782. doi: 10.1016/s0038-0717(98)00038-8
128. Newman, E. I., and Reddell, P. (1987). The distribution of mycorrhizas among families of vascular plants. New Phytol. 106, 745-751. doi: 10.1111/j.1469-8137.1987.tb00175.x
129. Oelze, V. M., Siebert, A., Nicklisch, N., Meller, H., Dresely, V., and Alt, K. W. (2011). Early Neolithic diet and animal husbandry: stable isotope evidence from three Linearbandkeramik (LBK) sites in Central Germany. J. Archaeol. Sci. 38, 270-279. doi: 10.1016/j.jas.2010.08.027
130. 15N. Biogeochemistry 80, 143-171. doi: 10.1007/s10533-006-9015-9
131. Parnell, A. C., Inger, R., Bearhop, S., and Jackson, A. L. (2010). Source partitioning using stable isotopes: coping with too much variation. PLoS ONE 5:e9672. doi: 10.1371/journal.pone.0009672
132. Petersen, S. O., Lind, A.-M., and Sommer, S. G. (1998). Nitrogen and organic matter losses during storage of cattle and pig manure. J. Agric. Sci. 130, 69-79. doi: 10.1017/S002185969700508X
133. Petzke, K. J., Boeing, H., Klaus, S., and Metges, C. C. (2005). Carbon and nitrogen stable isotopic composition of hair protein and amino acids can be used as biomarkers for animal-derived dietary protein intake in humans. J. Nutr. 135, 1515-1520.
134. 15N natural abundance in forest and pasture soils of the Brazilian Amazon Basin. Plant Soil 182,249-258. doi: 10.1007/BF00029056
135. Privat, K. L., O'Connell, T. C., and Richards, M. P. (2002). Stable isotope analysis of human and faunal remains from the Anglo-Saxon cemetery at Berinsfield, Oxfordshire: dietary and social implications. J. Archaeol. Sci. 29, 779-790. doi: 10.1006/jasc.2001.0785
136. 13C, 52H, 534S, and 518O values of orange fruit (Citrus sinensis L. Osbeck). J. Agric. Food Chem. 58,3502-3506. doi: 10.1021/jf903952v
137. Read, D. J. (1991). Mycorrhizas in ecosystems. Experientia 47, 376-391. doi: 10.1007/BF01972080
138. Regnell, M. (2002). “Charcoals from Uppakra as indicators of leaf fodder," in Centrality-Regionality. The Social Structure of Southern Sweden during the Iron Age, eds L. Larsson and B. Hardh (Stockholm: Almqvist & Wiksell International), 105-115.
139. Riga, A., Van Praag, H. J., and Brigode, N. (1971). Rapport isotopique naturel de l'azote dans quelques sols forestiers et agricoles de Belgique soumis a divers traitements culturaux. Geoderma 6, 213-222. doi: 10.1016/0016-7061(71)90064-4
140. 15N as an integrator of the nitrogen cycle. Trends Ecol. Evol. 16, 153-162. doi: 10.1016/S0169-5347(00)02098-X
141. 13C) to integrate the stress responses of wild barley (Hordeum spontaneum C. Koch.) genotypes. J. Exp. Bot. 51, 41-50. doi: 10.1093/jexbot/51.342.41
142. Ross, J. M., and Zutter, C. (2007). Comparing Norse animal husbandry practices: paleoethnobotanical analyses from Iceland and Greenland. ArcticAnthropol. 44, 62-85. doi: 10.3368/aa.44.1.62
143. Rowley-Conwy, P., and Layton, R. (2011). Foraging and farming as niche construction: stable and unstable adaptations. Philos. Trans. R. Soc. B Biol. Sci. 366, 849-862. doi: 10.1098/rstb.2010.0307
144. Ruess, R. W., and McNaughton, S. J. (1987). Grazing and the dynamics of nutrient and energy regulated microbial processes in the Serengeti grasslands. Oikos 49, 101-110. doi: 10.2307/3565559
145. Ruess, R. W., and McNaughton, S. J. (1988). Ammonia volatilization and the effects of large grazing mammals on nutrient loss from East African grasslands. Oecologia 77, 382-386. doi: 10.1007/BF00378047
146. Saito, L., Miller, W. W., Johnson, D. W., Qualls, R. G., Provencher, L., Carroll, E., et al. (2007). Fire effects on stable isotopes in a sierran forested watershed. J. Environ. Qual. 36, 91-100. doi: 10.2134/jeq2006.0233
147. Salvarina, I., Yohannes, E., Siemers, B. M., and Koselj, K. (2013). Advantages of using fecal samples for stable isotope analysis in bats: evidence from a triple isotopic experiment. Rapid Commun. Mass Spectrom. 27, 1945-1953. doi: 10.1002/rcm.6649
148. Schafer, J. L., and Mack, M. C. (2010). Short-term effects of fire on soil and plant nutrients in palmetto flatwoods. Plant Soil 334, 433-447. doi: 10.1007/s11104-010-0394-2
149. Schoeninger, M. J., and DeNiro, M. J. (1984). Nitrogen and carbon isotopic composition of bone collagen from marine and terrestrial animals. Geochim. Cosmochim. Acta 48, 625-639. doi: 10.1016/0016-7037(84) 90091-7
150. Schoeninger, M. J., DeNiro, M. J., and Tauber, H. (1983). Stable nitrogen isotope ratios of bone collagen reflect marine and terrestrial components of prehistoric human diet. Science 220, 1381-1383. doi: 10.1126/science.6344217
151. Schulze, E. D., Chapin, F. S., and Gebauer, G. (1994). Nitrogen nutrition and isotope differences among life forms at the northern treeline of Alaska. Oecologia 100, 406-412. doi: 10.1007/BF00317862
152. Schulze, E. D., Williams, R. J., Farquhar, G. D., Schulze, W., Langridge, J., Miller, J. M., et al. (1998). Carbon and nitrogen isotope discrimination and nitrogen nutrition of trees along a rainfall gradient in northern Australia. Aust. J. Plant Physiol. 25,413-425. doi: 10.1071/PP97113
153. Schwarcz, H. P., White, C. D., and Longstaffe, F. J. (2010). “Stable and radiogenic isotopes in biological archaeology: some applications," in Isoscapes: Understanding Movement, Pattern, and Process on Earth through Stable Isotope Mapping, eds J. B. West, G. J. Bowen, T. E. Dawson, and K. P. Tu (Heidelberg: Springer-Verlag), 335-356.
154. Schwertl, M., Auerswald, K., Schäufele, R., and Schnyder, H. (2005). Carbon and nitrogen stable isotope composition of cattle hair: ecological fingerprints of production systems? Agric. Ecosyst. Environ. 109, 153-165. doi: 10.1016/j.agee.2005.01.015
155. 15N abundance of soils associated with tillage practices. Can. J. Soil Sci. 64, 345-354. doi: 10.4141/cjss84-036
156. Shearer, G., Kohl, D. H., and Chien, S.-H. (1978). The nitrogen-15 abundance in a wide variety of soils. Soil Sci. Soc. Am. J. 42, 899-902. doi: 10.2136/sssaj1978.03615995004200060013x
157. Sherratt, A. (1980). Water, soil and seasonality in early cereal cultivation. World Archaeol. 11, 313-330. doi: 10.2307/124253
158. Silgram, M., and Shepherd, M. A. (1999). The effects of cultivation on soil nitrogen mineralization. Adv. Agron. 65,267-311. doi: 10.1016/s0065-2113(08)60915-3
159. Singer, F. J., and Schoenecker, K. A. (2003). Do ungulates accelerate or decelerate nitrogen cycling? Forest Ecol. Manag. 181, 189-204. doi: 10.1016/s0378-1127(03)00133-6
160. Sjögersten, S., Kuijper, D. P. J., Wal, R., Loonen, M. J. J. E., Huiskes, A. H. L., and Woodin, S. J. (2010). Nitrogen transfer between herbivores and their forage species. Polar Biol. 33, 1195-1203. doi: 10.1007/s00300-010-0809-9
161. 14N preferentially excreted? J. Archaeol. Sci. 30, 1649-1655. doi: 10.1016/s0305-4403(03)00066-9
162. 15Nfor tracer studies. J. Agric. Sci. 90, 7-9. doi: 10.1017/S002185960004853X
163. Steele, K. W., Wilson, A. T., and Saunders, W. M. H. (1981). Nitrogen isotope ratios in surface and sub-surface horizons of New Zealand improved grassland soils. N.Z. J. Agric. Res. 24, 167-170. doi: 10.1080/00288233.1981.10420885
164. 15N natural abundance values. Oecologia 101, 375-382. doi: 10.1007/BF00328825
165. 15N values as indicators of plant nitrogen metabolism. Phytochemistry 97, 20-29. doi: 10.1016/j.phytochem.2013.05.009
166. Styring, A. K., Manning, H., Fraser, R. A., Wallace, M., Jones, G., Charles, M., et al. (2013). The effect of charring and burial on the biochemical composition of cereal grains: investigating the integrity of archaeological plant material. J. Archaeol. Sci. 40, 4767-4779. doi: 10.1016/j.jas.2013.03.024
167. 15N abundances in the tissues and digesta of domestic animals. Radioisotopes 36, 74-77.
168. 15N in some components of ruminal fluid and plasma of sheep. J. Anim. Sci. 71, 226-231.
169. Szpak, P., Longstaffe, F. J., Millaire, J.-F., and White, C. D. (2012a). Stable isotope biogeochemistry of seabird guano fertilization: results from growth chamber studies with Maize (Zea mays). PLoS ONE 7:e33741. doi: 10.1371/jour-nal.pone.0033741
170. Szpak, P., Longstaffe, F. J., Millaire, J.-F., and White, C. D. (2014). Large variation in nitrogen isotopic composition of a fertilized legume. J. Archaeol. Sci. 45, 72-79. doi: 10.1016/j.jas.2014.02.007
171. Szpak, P., Millaire, J.-F., White, C. D., and Longstaffe, F. J. (2012b). Influence of seabird guano and camelid dung fertilization on the nitrogen isotopic composition of field-grown maize (Zea mays). J. Archaeol. Sci. 39, 3721-3740. doi: 10.1016/j.jas.2012.06.035
172. Szpak, P., Orchard, T. J., Mckechnie, I., and Gröcke, D. R. (2012c). Historical ecology of late Holocene sea otters (Enhydra lutris) from northern British Columbia: isotopic and zooarchaeological perspectives. J. Archaeol. Sci. 39, 1553-1571. doi: 10.1016/j.jas.2011.12.006
173. Szpak, P., White, C. D., Longstaffe, F. J., Millaire, J.-F., and Vásquez Sánchez, V. F. (2013). Carbon and nitrogen isotopic survey of northern Peruvian plants: baselines for paleodietary and paleoecological studies. PLoS ONE 8:e53763. doi: 10.1371/journal.pone.0053763
174. Ta, C. T., and Weiland, R. T. (1992). Nitrogen partitioning in maize during ear development. Crop Sci. 32, 443-451. doi: 10.2135/crop-sci1992.0011183X003200020032x
175. Tahir, I. S. A., and Nakata, N. (2005). Remobilization of nitrogen and carbohydrate from stems of bread wheat in response to heat stress during grain filling. J. Agron. Crop Sci. 191, 106-115. doi: 10.1111/j.1439-037X.2004. 00127.x
176. 15N-abundance in key metabolites? Funct. PlantBiol. 38, 1-12. doi: 10.1071/FP10091
177. Tiessen, H., Karamanos, R. E., Stewart, J. W. B., and Selles, F. (1984). Natural nitrogen-15 abundance as an indicator of soil organic matter transformations in native and cultivated soils. Soil Sci. Soc. Am. J. 48, 312-315. doi: 10.2136/sssaj1984.03615995004800020017x
178. Vaiglova, P., Bogaard, A., Collins, M., Cavanagh, W., Mee, C., Renard, J., et al. (2014). An integrated stable isotope study of plants and animals from Kouphovouno, southern Greece: a new look at Neolithic farming. J. Archaeol. Sci. 42,201-215. doi: 10.1016/j.jas.2013.10.023
179. 15N is affected by foliar nitrogen uptake, soil nitrogen, and mycorrhizae along a nitrogen deposition gradient. Oecologia 172,47-58. doi: 10.1007/s00442-012-2489-3
180. Van Groenigen, K.-J., Bloem, J., Bååth, E., Boeckx, P., Rousk, J., Bodé, S., et al. (2010). Abundance, production and stabilization of microbial biomass under conventional and reduced tillage. Soil Biol. Biochem. 42, 48-55. doi: 10.1016/j.soilbio.2009.09.023
181. Von Holstein, I. C. C., Hamilton, J., Craig, O. E., Newton, J., and Collins, M. J. (2012). Comparison of isotopic variability in proteinaceous tissues of adomesti-cated herbivore: a baseline for zooarchaeological investigation. Rapid Commun. Mass Spectrom. 27,2601-2615. doi: 10.1002/rcm.6725
182. Warinner, C., Garcia, N. R., and Tuross, N. (2013). Maize, beans and the floral isotopic diversity of highland Oaxaca, Mexico. J. Archaeol. Sci. 40, 868-873. doi: 10.1016/j.jas.2012.07.003
183. 15N abundance of plants and soils under different management practices in a montane grassland. Soil Biol. Biochem. 38, 1564-1576. doi: 10.1016/j.soilbio.2005.11.007
184. Werner, R. A., and Schmidt, H.-L. (2002). The in vivo nitrogen isotope discrimination among organic plant compounds. Phytochemistry 61, 465-484. doi: 10.1016/s0031-9422(02)00204-2
185. 15N fractionation between vegetation, soil, faeces and wool is not influenced by stocking rate. PlantSoil 340, 25-33. doi: 10.1007/s11104-010-0411-5
186. Wrage, N., Küchenmeister, F., and Isselstein, J. (2011). Isotopic composition of soil, vegetation or cattle hair no suitable indicator of nitrogen balances in permanent pasture. Nutr. Cycl. Agroecosyst. 90, 189-199. doi: 10.1007/s10705-011-9421-9
187. 15N abundance in soils and plants in relation to N cycling in a rangeland in Inner Mongolia. J. Plant Ecol. 3, 201-207. doi: 10.1093/jpe/rtq023
188. 14N fractionation during N2 fixation in the legume-rhizobia symbiotic system. Plant Cell Physiol. 27, 791-799.
189. 15N: progress over the last 30 years. Phytochem. Rev. 2, 121-132. doi: 10.1023/B:PHYT.0000004198.95836.ad
190. 15N in nitrogenous fractions of komatsuna plants supplied with nitrate. Plant Cell Physiol. 30, 957-962.
191. Yuan, Y., Zhao, M., Zhang, Z., Chen, T., Yang, G., and Wang, Q. (2012). Effect of different fertilizers on nitrogen isotope composition and nitrate content of Brassica campestris. J. Agric. Food Chem. 60, 1456-1460. doi: 10.1021/jf203105t
192. 15N abundance of paddy rice (Oryza sativa L.) grown with synthetic fertilizer, livestock manure compost, and hairy vetch. Biol. Fertil. Soils 47, 607-617. doi: 10.1007/s00374-011-0571-3
193. 15N abundance of plant and soil inorganic-N as evidence for over-fertilization with compost. Soil Biol. Biochem. 41, 1541-1547. doi: 10.1016/j.soilbio.2009.04.014
194. Yun, S.-I., Ro, H.-M., Choi, W.-J., and Chang, S. X. (2006). Interactive effects of N fertilizer source and timing of fertilization leave specific N isotopic sig-natures in Chinese cabbage and soil. Soil Biol. Biochem. 38, 1682-1689. doi: 10.1016/j.soilbio.2005.11.022
195. 15 N abundance in winter wheat amended with urea and compost: a long-term experiment. Pedosphere 23, 835-843. doi: 10.1016/s1002-0160(13)60075-2